Phyllomedusa 18(2):185–193, 2019 © 2019 Universidade de São Paulo - ESALQ ISSN 1519-1397 (print) / ISSN 2316-9079 (online) doi: http://dx.doi.org/10.11606/issn.2316-9079.v18i2p185-193 Delayed escape responses of male Basiliscus plumifrons (Squamata: Corytophanidae) during peak activity

Matthew S. Lattanzio Department of Organismal and Environmental Biology, Christopher Newport University. Newport News, Virginia 23606, USA. E-mail: [email protected].

Abstract Delayed escape responses of male Basiliscus plumifrons (Squamata: Corytophanidae) during peak activity. Many animals must balance their time spent active in a habitat against their perceived risk of predation. Factors that may increase that perceived risk, such as a faster predator approach, are therefore expected to cause prey to initiate escape quickly to avoid capture. At the same time, because patterns of daily activity can fuctuate throughout the day, the relative costs and benefts of initiating escape may also differ over time. Here I evaluated the escape responses of adult male emerald basilisk (Basiliscus plumifrons) lizards in two different time periods: morning (when daily activity peaks) and early afternoon (when activity is suppressed). Further, I approached each lizard at either a practiced slow or fast pace. Escape responses were recorded as fight-initiation (distance between observer and lizard prior to escape) and fight (distance travelled during escape) distance. No factor affected fight distance, and approach speed also had no effect on fight initiation distance. In contrast, time period affected fight initiation distance, with males approached in the morning delaying their escape response compared to males approached during the early afternoon. Because morning and early afternoon periods coincide with peak and suppressed periods of activity for basilisks at this study site, respectively, ambush- foraging species like B. plumifrons may delay escape when active to avoid prematurely alerting the predator of their presence.

Keywords: activity, Emerald Basilisk, fight distance, fight-initiation distance, lizard, optimal escape theory.

Resumo Respostas de fuga atrasadas de machos de Basiliscus plumifrons (Squamata: Corytophanidae) durante o pico de atividade. Muitos animais devem equilibrar o tempo gasto em atividade em um habitat com o risco de predação percebido. Portanto, espera-se que fatores que possam aumentar aquele risco, como uma aproximação mais rápida do predador, façam com que a presa inicie a fuga

Received 04 January 2019 Accepted 12 August 2019 Distributed December 2019

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rapidamente para evitar a captura. Ao mesmo tempo, como os padrões de atividade diária podem variar ao longo do dia, os custos e benefícios relativos de iniciar a fuga também podem diferir ao longo do tempo. Avaliei aqui as respostas de fuga de machos adultos do basilisco-esmeralda (Basiliscus plumifrons) em dois períodos diferentes: manhã (quando a atividade diária atinge o pico) e início da tarde (quando a atividade cessa). Além disso, eu me aproximei de cada lagarto a passos lentos ou rápidos. As respostas de fuga foram registradas como distância de início de fuga (distância entre o observador e o lagarto antes da fuga) e distância de fuga (distância percorrida durante a fuga). Nenhum fator afetou a distância de fuga e a velocidade de aproximação também não teve efeito sobre a distância de início de fuga. Por outro lado, o período de tempo afetou a distância de início de fuga, com os machos abordados de manhã atrasando sua resposta de fuga em comparação com os machos abordados no início da tarde. Como os períodos da manhã e do início da tarde coincidem, respectivamente, com os períodos de atividade máxima e de cessação da atividade para os basiliscos neste local de estudo, predadores de tocaia como B. plumifrons podem atrasar a fuga quando ativos para evitar alertar prematuramente o predador sobre sua presença.

Palavras-chave: atividade, basilisco-esmeralda, distância de fuga, distância de iniciação da fuga, lagarto, teoria da fuga ótima.

Introduction 2007, Cooper Jr. et al. 2009, Lattanzio 2009, 2014, Brock et al. 2015, Stellatelli et al. 2015). How a prey organism responds to an Many factors affecting variation in FID and approaching predator has clear and immediate FD by lizards have been identifed (reviewed by ftness consequences (Ydenberg and Dill 1986), Stankowich and Blumstein 2005, Samia et al. and it is therefore unsurprising that these 2015). For example, individuals that perceive a responses are well-studied in many taxa greater risk of predation often initiate the escape (reviewed by Stankowich and Blumstein 2005). response earlier (i.e., at a greater FID) and fee A major component of the anti-predation further than individuals which perceive lesser response in lizards, their escape behavior, is risk (Ydenberg and Dill 1986). One relatively often modeled in an economic fashion because underappreciated factor that may affect that of the cost-beneft trade-offs surrounding the perception of risk is their level or type of activity decisions of when and how far to fee an at the time of a predatory encounter (Cooper Jr. approaching predator (e.g., Ydenberg and Dill and Pérez-Mellado 2004, Cooper Jr. 2009). 1986, Cooper Jr. and Blumstein 2015). This Specifcally, many species vary in their frequency process can be quantifed by estimating two and use of different behaviors throughout the parameters: fight-initiation distance and fight day, and so shunting energy from other behaviors distance (FID and FD respectively). Briefy, FID to an antipredator response requires consideration represents the distance between an approaching of the potential costs of that energetic trade-off. predator and the lizard prior to its escape and FD For example, during periods of foraging, the is the distance fed by the lizard during the initial costs of giving up access to resources (food) escape response (e.g., Lailvaux et al. 2003, may lead an individual lizard to delay its escape Cooper Jr. and Frederick 2007). Empirical response (Cooper Jr. et al. 2006). In addition to studies have revealed strong support for this food resources, temperature variability also model across several lizard taxa, supporting its contributes to shaping variation in daily activity utility for understanding the factors affecting patterns in lizards (Adolph and Porter 1993) and, escape decisions by this diverse clade (Cooper unsurprisingly, has been associated with Jr. 2003a, Martín 2003, Vanhooydonck et al. variation in their escape decisions as well (e.g.,

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Rocha and Bergallo 1990). Given these considerations, it stands to reason that daily variation in patterns of activity may also coincide with similar variability in escape responses (Lattanzio 2014). The speed of a predator’s approach may also infuence escape decisions (Stankowich and Blumstein 2005). For example, predator approach speed could serve as a cue to a prey species regarding whether or not it has been detected (Cooper Jr. 2006). In addition, faster approaches reduce the time until a predator reaches its Figure 1. Male emerald basilisk (Basiliscus plumifrons) potential prey, which affects their time to initiate from El Zota Biological Field Station in Costa an escape response as well as the likelihood of Rica. Photograph by Matthew S. Lattanzio. success of that response (Cooper Jr. 2003a, 2003b). The escape responses of lizards should be susceptible to variable predator approach speeds (Stankowich and Blumstein 2005), and some Materials and Methods studies have shown that faster approaches do elicit a more-rapid prey response (e.g., greater The Emerald Basilisk (Basiliscus plumifrons; FID, reviewed by Samia et al. 2015; but see Figure 1) is one of four currently recognized Lattanzio 2009). Unlike FID, however, FD may species of basilisk lizard (Corytophanidae: not be as sensitive to variation in predator Basiliscus; see Maturana 1962). These species approach speed (e.g., Lattanzio 2009). have a scattered, often overlapping distribution Here I describe variation in the escape along the rainforests of Central and South behavior (FID and FD) of adult male emerald America. Basiliscus plumifrons is a medium- basilisk (Basiliscus plumifrons Cope, 1875; sized, semi-arboreal lizard common throughout Figure 1) lizards in northeastern Costa Rica with lowland moist forests of Costa Rica, Nicaragua, respect to two factors, time of day (morning or Panama, and Honduras (Wilson et al. 2013). early afternoon) and speed of approach (slow or Although primarily insectivorous, adult basilisks fast). Both factors are known to infuence the have been observed to also eat fruit, fowers, and escape behavior in other lizard species (Cooper even smaller vertebrates (Hirth 1963). Juvenile Jr. 2003a, 2006, Lattanzio 2014). I use time of basilisks are commonly found along rivers, day as a proxy for basilisk activity in this study streams, lakes, and other waterways, where they because their activity exhibits a bimodal can best make use of their unique escape strategy distribution with respect to time of day at my of running across water surfaces (Savage 2002). study site, with an initial peak in the early Adults, which are unable to use this behavior as morning, followed by a suppression of activity effectively as juveniles (Hsieh and Lauder 2004), until peaking again in the late afternoon hours are often observed in areas greater than 30 m (Lattanzio and LaDuke 2012). In accordance from water sources at this site (Lattanzio, pers. with theory (Ydenberg and Dill 1986), and the obs.). fndings of previous studies (Cooper Jr. et al. I observed the escape responses of 17 adult 2006, Lattanzio and LaDuke 2012), I predicted male (> 115 mm snout–vent length; Laerm 1974) that those B. plumifrons approached in the early B. plumifrons from 19–24 July 2005 at El Zota afternoon, and those approached at a faster Biological Field Station in Costa Rica (10.55728° speed, would fee earlier and further. N, 83.73628° W) (Pruetz and LaDuke 2001).

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Males are easily discerned from females by the All analyses were conducted within the R presence of dorsal and caudal crests (males-only, software environment (R Development Core see Figure 1). This station encompasses Team 2012). Using Shapiro-Wilk’s tests approximately 1000 ha of a mosaic of primary (function ‘shapiro.test’ in the stats package), I and secondary rainforest habitats. Basilisks found that raw FID (W = 0.91, p = 0.11), but not frequent secondary and edge habitats throughout FD (W = 0.7, p < 0.001), met assumptions of the southeastern portion of El Zota (Lattanzio normality. In addition, FID and FD were and LaDuke 2012). I therefore conducted this uncorrelated [Spearman’s rho (function ‘cor.test’ study along trail and road edges within the in stats package), ρ = -0.38, S = 1126, N = 17, station. p = 0.13]. I therefore analyzed each escape I used binoculars to initially sight lizards response (FID, FD) in a separate test. For FID, I from a distance (>10 m) to minimize disturbing used a factorial analysis of variance (ANOVA, my focal animals prior to data collection. In function ‘aov’ in stats package) with time of day addition, I only approached lizards that were not (morning or early afternoon) and approach speed already moving to minimize error in distance (slow or fast) as fxed effects. I ranked values of measurements. Upon locating a focal lizard, I FD using the function ‘rank’ in the base R then acted as a simulated predator by walking a package; these ranked FID values satisfed direct, straight path towards the animal. I normality assumptions (Shapiro-Wilks test, W = recorded FID and FD to the nearest 0.1 m using 0.96, p = 0.67). I then applied a factorial ANOVA a tape measure. on the ranked FD values against the same I investigated the effect of two parameters predictors included in the FID model. I likely to infuence antipredator decisions on the interpreted outputs of both models using Type II escape responses of B. plumifrons: time of day ANOVA tables via the function ‘Anova’ in the and approach speed (Cooper Jr. 2003a, Lattanzio car package (Fox and Weisberg 2011). Residuals 2014). To investigate how time of day affects B. from both models satisfed normality assumptions plumifrons escape decisions, I approached (Shapiro-Wilks test, FID model: W = 0.97, p = lizards either during the morning (08:00–10:00 0.8; FD model: W = 0.94, p = 0.33). I also h, N = 8 lizards) or early afternoon (12:00–14:00 confrmed homogeneity of variances for each h, N = 9 lizards). All lizards were perched on model using the function ‘leveneTest’ in the car similar substrates (branches of small shrubs) package (Fox and Weisberg 2011) (FID prior to my approach. I chose these survey model: F3,13 = 0.52, p = 0.68; FD model: F3,13 = periods based on observations from a concurrent 0.27, p = 0.84). Means are presented ± 1 standard study on the bimodal daily activity patterns of deviation in text. other B. plumifrons lizards in this area: adult activity peaks closer to dawn and dusk later in Results July (Lattanzio and LaDuke 2012). My time periods therefore provide a useful contrast of B. In general, males approached in the morning plumifrons activity, with a period of high had lower FID values than males approached in (morning) and low (early afternoon) activity. I the early afternoon (morning FID = 2.85 ± 0.9 approached lizards at one of two practiced, m; early afternoon FID = 4.64 ± 1.6 m). controlled paces: slow (~ 50 m/min) or fast Approach speed, however, had little if any (~ 150 m/min), following Lattanzio (2009). impact on lizard FID (slow pace FID = 3.72 ± I conducted all surveys on sunny days, wore 1.2 m; fast pace FID = 3.89 ± 2 m). My model similarly-colored clothing throughout my supported a signifcant effect of time of day on experiment, and never explored the same area male FID (time of day: F1,13 = 7.04, p = 0.02; twice to avoid pseudoreplication. approach speed: F1,13 = 0.23, p = 0.64; time of

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day × approach speed: F1,13 = 0.73, p = 0.41), with males feeing sooner in the early afternoon than in the morning hours (Figure 2). In terms of FD, males approached in the morning appeared to fee further than males approached in the early afternoon (morning FD = 2.63 ± 1.9 m; early afternoon FD = 1.73 ± 0.7 m). Approach speed also appeared to impact FD, with faster approach coinciding with greater FD (slow pace FD = 1.86 ± 0.7 m; face pace FD = 2.48 ± 1.9 m). However, my model revealed that neither time of day nor approach speed had a signifcant effect on FD

(time of day: F1,13 = 1.1, p = 0.31; approach speed: F1,13 = 0.02, p = 0.88; time of day × Figure 2. Variation in flight-initiation distance (in meters) by time of day, morning (08:00–10:00 h) or approach speed: F1,13 = 1.42, p = 0.26). early afternoon (12:00–14:00 h) by adult B. Discussion plumifrons observed in this study. Medians are represented by the black central horizontal bar and means are indicated by the symbol Basilisks, like other ambush foraging lizards, ‘×’. budget the energetic demands of territorial patrol and foraging behavior with alternative needs, such as antipredator behavior (Watters 2009). I quantifed a component of antipredator behavior, infuence of non-antipredator behaviors on the escape response, of adult male emerald escape decisions has received scant attention basilisk lizards with respect to variation in time compared to other driving factors like the of day and approach speed, both of which may characteristics of a predator’s approach (reviewed infuence perceived risk in lizards (Cooper Jr. by Stankowich and Blumstein 2005). Thus far, 2006, Lattanzio 2014). Despite my predictions, I both social and foraging activity have been found no effect of approach speed on fight found to infuence fight-initiation distance in initiation distance, and no effect of either time lizards (Cooper Jr. et al. 2006, Cooper Jr. 2009). period or speed on distance fed. However, my Moreover, in another tropical lizard species, prediction regarding the infuence of time of day Holcosus festivus (Lichtenstein and Martens, on fight initiation distance was supported, as 1856) (= Ameiva festiva), daily patterns of lizards fed sooner in the early afternoon than in general activity also seem to have an impact on the morning hours (see Figure 2). Because the escape response thresholds throughout the day time periods of surveys used in my study (Lattanzio 2014). In this study, I found that B. correspond directly to a peak (morning) and plumifrons lizards allowed a closer approach valley (early afternoon) in B. plumifrons activity during periods of peak activity (morning), which at my study site (Lattanzio and LaDuke 2012), supports that activity may infuence escape these fndings suggest that adult activity levels behavior. may affect risk perception in this species. Interestingly, these fndings contrast with The type of activity exhibited by a prey escape patterns observed in a previous study on organism during a predator’s approach, and its an active-foraging species, H. festivus (Lattanzio energetic benefts, should infuence the threshold 2014). Unlike ambush foragers like B. plumifrons of risk associated with the decision of when to which move infrequently and remain perched for initiate an escape response. However, the extended periods of time while scanning for

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potential food, mates, or territory intruders, approaches, so any conclusions about the direct active foragers like H. festivus exhibit frequent association of these environmental conditions (or and sporadic movement that increases their risk others) with lizard escape behavior would be of drawing unwanted attention from nearby speculative. I thus encourage others to consider predators (Broom and Ruxton 2005). Thus, thermal ecology of B. plumifrons in future escape during periods of peak activity, species differing studies to better disentangle the role of activity in foraging strategies should also differ in patterns versus thermal constraints on shaping whether they fee sooner (active foragers) or diel variation in their escape decisions. later (ambush foragers) once an approaching Additional data on both active and ambush predator is detected (Lattanzio 2014). In support foraging species alike will also provide important of this hypothesis, B. plumifrons in this study insight into the extent that any differences in allowed closer approaches during the morning, their escape tactics, or relationships between one of two periods during the day where they their escape behavior and activity patterns or exhibit heightened periods of activity this time temperature, mirror their divergent foraging of year (see Lattanzio and LaDuke 2012). Much strategies. of the activity of this species at El Zota appears Unlike time of day, I found no effect of the to be temperature-dependent, as activity period speed of my approach on any escape responses peaks shift throughout the summer months to of B. plumifrons. Numerous studies support that cooler morning and late afternoon time periods approach speed can be an important risk factor (Lattanzio and LaDuke 2012). My current affecting the escape responses of multiple fndings suggest that their daily patterns of species (e.g., Cooper Jr. 1997, 2003a, Cooper Jr. escape response thresholds may shift as well. and Whiting 2007a, 2007b, Cooper Jr. et al. However, it is important to also recognize the 2009, but see also Lattanzio 2009). My methods infuence of temperature on both lizard activity are consistent with other studies (e.g., practiced in general and, at least in some species, escape approach speeds, similarly-colored clothing responses (Rocha and Bergallo 1990, Adolph worn during all trials, etc.), and my approach and Porter 1993). For example, during periods of speeds fall within the range of other published warmer air temperatures (such as afternoon studies (broader range: 40–180 m/min; e.g., hours), activity may be suppressed to conserve Cooper Jr. 1997, 2003a), suggesting that a lack energy (Kearney 2013). By that logic, a delayed of response to approach speed by B. plumifrons escape response should also be benefcial under is likely not due to sampling error. Alternatively, these conditions to minimize the energetic costs because ambush foragers like B. plumifrons rely of movement until predator attack is imminent. on crypsis to avoid predator detection and move One means to gain preliminary insight into infrequently, it may simply be that escape the relative infuence of activity patterns and responses are a primary function of detection by temperature on escape responses would be to (rather than the speed of) an approaching record air and substrate temperatures during an predator for these taxa (Broom and Ruxton escape study and include those variables in data 2005). However, given the relatively small analyses as covariates. To that end, the results of sample size of my study, more work is needed to previous studies are mixed with respect to the evaluate this claim. potential effect of temperature on escape In general, faster approach speeds are responses, suggesting any effect may be species- expected to elicit sooner prey responses (and specifc and not universal (Blamires 1999, thus greater fight-initiation distances) because a Stankowich and Blumstein 2005, Braun et al. fast-approaching predator has likely detected the 2010). It is important to note that I did not record prey (e.g., Cooper Jr. 1997). However, this cue air or substrate temperature data during my may be more important for active foragers whose

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frequent movement alone may attract predator In truth, unlike approach speed, the distance attention, compared to ambush foragers that rely between a predator and prey has consistent and on crypsis or proximity to a refuge to minimize strong ftness implications, regardless of other detection (Cooper Jr. 2005). Moreover, it is also risk factors: as this distance approaches zero, important to note that models predicting the risk of mortality for a prey animal rises strategies for cryptic prey argue that slower, not rapidly towards 100%. Thus, for cryptic prey faster, predator search speeds should elicit an species, distance to a predator may be a stronger earlier escape response (Broom and Ruxton cue for the initiation of an escape response than 2005). Taken together, these studies suggest that the speed of a predator’s approach. One outcome prey responses may be complex and depend of this consideration would be the prey animal upon whether the prey perceives a positive eliciting similar escape responses regardless of correlation between approach speed and predator approach speed variation, as was detection probability (Cooper Jr. 1997, Broom observed for B. plumifrons in the current study. and Ruxton 2005), which may be limited to There may also be a regional effect, as both actively-foraging taxa. Lattanzio (2009) and this study were conducted Thus far, support for this foraging mode at the same feld station (but on different species hypothesis remains mixed. In general, the in different portions of the station property). responses of many active foraging species Thus, lizards may be more accustomed to human support a clear effect of approach speed on fight presence at El Zota than they would be in other initiation distance: Cnemidophorus murinus areas (e.g., Labra and Leonard 1999, Diego- (Laurenti, 1768) (Cooper Jr. et al. 2003); Rasilla 2003, Prosser et al. 2006). Data on a Cordylus niger Cuvier, 1829 (Cooper Jr. and wider array of taxa along a broader gradient of Whiting 2007b); Dipsosaurus dorsalis (Baird human disturbance would be useful in this and Girard, 1852) (Cooper Jr. 2003a); Eumeces respect to better understand the implications of laticeps (Schneider, 1801) (Cooper Jr. 1997); predator approach characteristics for prey Podarcis lilfordi (Günther, 1874) (Cooper Jr. et behavior. al. 2009); Psammodromus algirus (Linnaeus, 1758) (Martín and López 1996); Rhoptropus Acknowledgments boultoni Schmidt, 1933 (Cooper Jr. and Whiting 2007a); Trachylepis acutilabris (Peters, 1862) (= I thank Thomas LaDuke as well as DANTA Mabuya acutilabris) (Cooper Jr. and Whiting Association for Conservation of the Tropics for 2007a); and Trachylepis sparsa (Mertens, 1954) providing access to the feld site and materials (Cooper Jr. and Whiting 2007b). However, of used to conduct this study. I also respectfully seven ambush foraging species studied to date, acknowledge the station workers, José, Ana, only three species ft expectations and were and their family at El Zota Biological Field unaffected by approach speed: Anolis limifrons Cope, 1862 (=Norops limifrons) and Anolis Station for their on-site assistance and humilis Peters, 1863 (= Norops humilis) accommodations. I am further indebted to (Lattanzio 2009); and B. plumifrons (this study). Casey Fox and John Scrivo for assistance in the The responses of the other four ambush-foraging feld. This work was conducted in full species (Agama planiceps Peters, 1862; Anolis compliance with all applicable institutional lineatopus Gray, 1840; Holbrookia propinqua animal care and use guidelines set forth by East Baird and Girard, 1852; and Sceloporus virgatus Stroudsburg University, and under a wildlife Smith, 1938) fed sooner when approached at a research permit issued to my advisor (TCL) by faster pace (Cooper Jr. 2003b, 2005, 2006, the Costa Rican Ministerio del Ambiente, Cooper Jr. and Whiting 2007a). Energia y Telecomunucaciones.

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